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This Article Appeared in a Journal Published by Elsevier. the Attached This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy C. R. Biologies 334 (2011) 737–741 Contents lists available at ScienceDirect Comptes Rendus Biologies ww w.sciencedirect.com Animal biology and pathology/Biologie et pathologie animales Blochmannia endosymbionts and their host, the ant Camponotus fellah: Cuticular hydrocarbons and melanization Relations entre endosymbiotes Blochmannia et leur hoˆte, la fourmi Camponotus fellah avec hydrocarbures cuticulaires et me´lanisation a,b, a a, Danival Jose´ de Souza *, Se´verine Devers , Alain Lenoir * a IRBI, institut de recherche sur la biologie de l’insecte, UMR CNRS 6035, universite´ Franc¸ois-Rabelais, parc de Grandmont, 37200 Tours, France b Fundac¸a˜o Universidade Federal do Tocantins, Campus Universita´rio de Gurupi, Rua Badejo´s, 77402-970, Gurupi, TO, Brazil A R T I C L E I N F O A B S T R A C T Article history: Carpenter ants (genus Camponotus) have mutualistic, endosymbiotic bacteria of the genus Received 13 January 2011 Blochmannia whose main contribution to their hosts is alimentary. It was also recently Accepted after revision 23 June 2011 demonstrated that they play a role in improving immune function as well. In this study, we Available online 24 August 2011 show that treatment with an antibiotic produces a physiological response inducing an increase in both the quantity of cuticular hydrocarbons and in the melanization of the Keywords: cuticle probably due to a nutritive and immunological deficit. We suggest that this is Blochmannia because it enhances the protection the cuticle provides from desiccation and also from Cuticular hydrocarbons invasions by pathogens and parasites. Nevertheless, the cuticular hydrocarbon profile is Antibiotic not modified by the antibiotic treatment, which indicates that nestmate recognition is not Melanization modified. Endosymbiotic bacteria ß 2011 Acade´mie des sciences. Published by Elsevier Masson SAS. All rights reserved. Carpenter ants R E´ S U M E´ Mots cle´s : Les fourmis charpentie`res (du genre Camponotus) posse`dent des bacte´ries endosymbio- Blochmannia tiques mutualistes du genre Blochmannia qui contribuent a` l’alimentation de leurs hoˆtes. Il Hydrocarbures cuticulaires a e´te´ de´montre´ re´cemment qu’elles peuvent aussi favoriser les re´ponses immunitaires. Antibiotiques Dans cette e´tude, nous montrons qu’a` la suite d’un traitement antibiotique, les fourmis ont Me´lanisation une re´ponse physiologique induisant la production de plus d’hydrocarbures cuticulaires et Bacte´ries endosymbiotiques une cuticule plus me´lanise´e. Cela doit permettre une protection contre la perte d’eau et Fourmis charpentie`res pre´venir mieux contre l’intrusion de pathoge`nes et parasites. Ne´anmoins, le profil d’hydrocarbures cuticulaires n’est pas modifie´ par le traitement antibiotique, ce qui permet le maintien de la reconnaissance des conge´ne`res du nid. ß 2011 Acade´mie des sciences. Publie´ par Elsevier Masson SAS. Tous droits re´serve´s. 1. Introduction studied thus far [1,2]. The function of endosymbionts has not totally been elucidated, but their role in supplying Carpenter ants (genus Camponotus) have established an complementary dietary nitrogen was shown through the association with the intracellular endosymbiont Bloch- analysis of the genome sequence of two species of mannia (g-Proteobacteria) found in all of the species Blochmannia [1,3–5] and in experiments eliminating the bacteria through the administration of antibiotics and the use of chemically–based diets [6,7]. However, the apparent ability of the ants to survive without Blochmannia and the * Corresponding author. E-mail address: [email protected] (A. Lenoir). omnivorous behaviour of several Camponotus species 1631-0691/$ – see front matter ß 2011 Acade´mie des sciences. Published by Elsevier Masson SAS. All rights reserved. doi:10.1016/j.crvi.2011.06.008 Author's personal copy 738 D. Jose´ de Souza et al. / C. R. Biologies 334 (2011) 737–741 suggests that the bacteria perform other functions for the 2.3. Chemical analyses ants. We recently demonstrated that the presence of Blochmannia may be important during the colony-found- Parts (i.e., the head and thorax, including the legs) taken ing phase, and that these bacteria play a role in improving from 27 treated workers and 31 control ants were the immune response of the ants [8]. immersed in 1 mL of pentane for 5 min and then removed, Here, we tested other functions the bacterial endosym- and 5 ml of pentane containing 50 ng of eicosane (C20) was biont carries out for the host ants. It is well known that added as an internal standard. For the analyses, the solvent cuticular surface chemicals, mainly hydrocarbons, protect was evaporated until 5 ml remained which were then insects from desiccation [9,10]. These hydrocarbons also injected into an FID gas chromatograph (VGM250Q play an underestimated role in providing protection from system, Perkin-Elmer) using a DB-5 fused silica capillary pathogens [11]. We tested the effects of an antibiotic column. The temperature was kept at 150 8C during the treatment in eliminating or greatly reducing the quantity splitless initial 2 min, raised from 150 8C to 310 8C at 5 8C/ of endosymbiotic bacteria on the cuticles of the ants and on min and held at 310 8C for the last 10 min. The cuticular the melanization processes. hydrocarbons had been previously identified [13,14]. To also identify the smaller peaks, we analyzed the cuticular profile in greater detail with the same gas chromatograph 2. Material and methods coupled to a Perkin-Elmer mass spectrometer operating at 70 eV. We used a high temperature column to identify the 2.1. The ants peaks with more than 30 carbons (DB-5HT, 30 m, 0.251 mm  0.10 mm). The temperature program was Incipient colonies of Camponotus fellah were collected 2 min at 100 8C; 6 8C/min until 350 8C and maintained by Pr Abraham Hefetz in Tel-Aviv in March 2007. The for 5 min. The areas of the peaks were estimated through colonies were placed into plastic containers peak integration using a TurboChrome Workstation. We (20  20  10 cm) furnished with plaster nests and kept then calculated the quantities of substances using the in a climate chamber (constant temperature of 28 8C, 12 h internal standard area (ng per thorax) and their relative DL), and were fed twice a week with Tenebrio molitor larvae proportions. Hydrocarbon classes by percentage and total and honey. Each colony contained one queen, and at least quantities were compared with the Mann-Whitney U test. one hundred workers and brood. We used 10 control Data expressed as a percentage are used with the Arcsine colonies (also fed with Tenebrio larvae and honey) and 10 (square root) transformation [15]. The profiles between treatment colonies (fed with Tenebrio larvae and honey for the two groups were compared with a dendrogram using the first week, and then Tenebrio larvae and honey solution the single-link Ward method and Euclidian distance. containing 1% of the antibiotic rifampicin for the second week and thereafter). The treatment was applied during 3 3. Results months. It has previously been shown that the antibiotic treatment has no side effects on medium-sized ants (see 3.1. Degree of melanization Discussion in [6,8]). For the experiments, we used medium-sized foraging workers selected randomly from Antibiotic-treated ants showed a significant increase in all of the colonies. We verified that there was no detectable the degree of melanization when compared to the control colony effect. In previous studies, we confirmed the group (Student’s t-test, t26 = 12.9, P < 0.00001; Fig. 1). efficacy of the antibiotic treatment in eliminating bacteria Treated ants exhibited a degree of melanization approxi- using real-time quantitative polymerase chain reaction mately two times superior to that of control ants. (PCR) and fluorescence in situ hybridization (FISH) tests. It was demonstrated that the antibiotic treatment reduced 3.2. Chemical analysis the amount of bacteria by at least 75% [8]. We recorded 62 peaks, of which 58 were identified. Our 2.2. Degree of melanization of the cuticle analysis was very detailed as 43 out of the 58 had not We dissected the third tergite from 27 naive workers and 29 workers treated with antibiotics. They were placed TM in Clarion medium, and then mounted on glass slides. Each piece was examined under a light microscope and photographed using a digital camera (Olympus DP50). The mean grey value of the cuticle fragment was measured using ImageJ 1.37v software. The background grey value was subtracted to correct the values of the fragments. The mean grey value was obtained by measuring three square plots in each figure. We assumed that the darkest grey corresponded to the cuticle with the highest degree (i.e., totally black) of melanization. Melanization is normally achieved a few days after imaginal eclosion, but changes Fig. 1. Means (Æ SE) of the degree of melanisation of the cuticle on control occur in adults, for example, as they age [12]. (n = 27) and antibiotic-treated ants (n = 29). Student’s t-test, P < 0.0001.
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